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Microbial metabolic exchange—the chemotype-to-phenotype link

Abstract

The function of microbial interactions is to enable microorganisms to survive by establishing a homeostasis between microbial neighbors and local environments. A microorganism can respond to environmental stimuli using metabolic exchange—the transfer of molecular factors, including small molecules and proteins. Microbial interactions not only influence the survival of the microbes but also have roles in morphological and developmental processes of the organisms themselves and their neighbors. This, in turn, shapes the entire habitat of these organisms. Here we highlight our current understanding of metabolic exchange as well as the emergence of new technologies that are allowing us to eavesdrop on microbial conversations comprising dozens to hundreds of secreted metabolites that control the behavior, survival and differentiation of members of the community. The goal of the rapidly advancing field studying multifactorial metabolic exchange is to devise a microbial 'Rosetta stone' in order to understand the language by which microbial interactions are negotiated and, ultimately, to control the outcome of these conversations.

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Figure 1: Microbial interactions.
Figure 2: Percentages of the predicted ORFs used in microbial interactions.
Figure 3: Chemical diversity of quorum-sensing molecules.
Figure 4: Chemical diversity of metabolic exchange factors.
Figure 5: Cell differentiation of Bacillus subtilis at the colony and cellular levels.
Figure 6: Ecological roles of microbial metabolic exchange.
Figure 7: MALDI-IMS links chemistry to bacterial phenotypes.

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References

  1. Newman, D.J. & Cragg, G.M. Natural products as sources of new drugs over the last 25 years. J. Nat. Prod. 70, 461–477 (2007).

    Article  CAS  PubMed  Google Scholar 

  2. Banat, I.M., Makkar, R.S. & Cameotra, S.S. Potential commercial applications of microbial surfactants. Appl. Microbiol. Biotechnol. 53, 495–508 (2000).

    CAS  PubMed  Google Scholar 

  3. Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).

    CAS  PubMed  Google Scholar 

  4. Hasan, F., Shah, A.A. & Hameed, A. Industrial applications of microbial lipases. Enzyme Microb. Technol. 39, 235–251 (2006).

    CAS  Google Scholar 

  5. Fujinami, S. & Fujisawa, M. Industrial applications of alkaliphiles and their enzymes–past, present and future. Environ. Technol. 31, 845–856 (2010).

    CAS  PubMed  Google Scholar 

  6. Fusetani, N. Antifouling marine natural products. Nat. Prod. Rep. 28, 400–410 (2011).

    CAS  PubMed  Google Scholar 

  7. Dayan, F.E., Cantrell, C.L. & Duke, S.O. Natural products in crop protection. Bioorg. Med. Chem. 17, 4022–4034 (2009).

    CAS  PubMed  Google Scholar 

  8. Babalola, O.O. Beneficial bacteria of agricultural importance. Biotechnol. Lett. 32, 1559–1570 (2010).

    CAS  PubMed  Google Scholar 

  9. Omura, S. et al. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. USA 98, 12215–12220 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Ikeda, H. et al. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21, 526–531 (2003).

    PubMed  Google Scholar 

  11. Bentley, S.D. et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147 (2002).

    PubMed  Google Scholar 

  12. Ohnishi, Y. et al. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J. Bacteriol. 190, 4050–4060 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Nett, M., Ikeda, H. & Moore, B.S. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep. 26, 1362–1384 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Snyder, E.E. et al. PATRIC: the VBI PathoSystems Resource Integration Center. Nucleic Acids Res. 35, D401–D406 (2007).

    CAS  PubMed  Google Scholar 

  15. Lowery, C.A., Dickerson, T.J. & Janda, K.D. Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem. Soc. Rev. 37, 1337–1346 (2008).

    CAS  PubMed  Google Scholar 

  16. Straight, P.D. & Kolter, R. Interspecies chemical communication in bacterial development. Annu. Rev. Microbiol. 63, 99–118 (2009). This review discusses the influence that a bacterium has within a community through participating in metabolic exchange.

    CAS  PubMed  Google Scholar 

  17. Ng, W.L. & Bassler, B.L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43, 197–222 (2009). This paper discusses the quorum-sensing networks in Vibrio spp.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Schuster, M. & Greenberg, E.P. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296, 73–81 (2006). This work discusses quorum-sensing regulation in P. aeruginosa.

    CAS  PubMed  Google Scholar 

  19. Antunes, L.C., Ferreira, R.B., Buckner, M.M. & Finlay, B.B. Quorum sensing in bacterial virulence. Microbiology 156, 2271–2282 (2010).

    CAS  PubMed  Google Scholar 

  20. Little, A.E., Robinson, C.J., Peterson, S.B., Raffa, K.F. & Handelsman, J. Rules of engagement: interspecies interactions that regulate microbial communities. Annu. Rev. Microbiol. 62, 375–401 (2008).

    CAS  PubMed  Google Scholar 

  21. Kaeberlein, T., Lewis, K. & Epstein, S.S. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296, 1127–1129 (2002).

    CAS  PubMed  Google Scholar 

  22. D'Onofrio, A. et al. Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem. Biol. 17, 254–264 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Lewis, K., Epstein, S., D'Onofrio, A. & Ling, L.L. Uncultured microorganisms as a source of secondary metabolites. J. Antibiot. (Tokyo) 63, 468–476 (2010).

    CAS  Google Scholar 

  24. Rigali, S. et al. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 9, 670–675 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. van Wezel, G.P. & McDowall, K.J. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat. Prod. Rep. 28, 1311–1333 (2011).

    CAS  PubMed  Google Scholar 

  26. López, D. & Kolter, R. Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol. Rev. 34, 134–149 (2010). This review discusses the cascades of cell differentiation pathways that are triggered by metabolic exchange.

    PubMed  Google Scholar 

  27. Straight, P.D., Willey, J.M. & Kolter, R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J. Bacteriol. 188, 4918–4925 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Angelini, T.E., Roper, M., Kolter, R., Weitz, D.A. & Brenner, M.P. Bacillus subtilis spreads by surfing on waves of surfactant. Proc. Natl. Acad. Sci. USA 106, 18109–18113 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Davies, J. Everything depends on everything else. Clin. Microbiol. Infect. 15 (suppl. 1): 1–4 (2009).

    PubMed  Google Scholar 

  30. Yim, G., Wang, H.H. & Davies, J. Antibiotics as signalling molecules. Phil. Trans. R. Soc. Lond. B 362, 1195–1200 (2007).

    CAS  Google Scholar 

  31. Fajardo, A. & Martinez, J.L. Antibiotics as signals that trigger specific bacterial responses. Curr. Opin. Microbiol. 11, 161–167 (2008).

    CAS  PubMed  Google Scholar 

  32. Shapiro, J.A. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104 (1998). This review is one of the first to discuss bacterial populations as multidimensional organisms.

    CAS  PubMed  Google Scholar 

  33. Strauss, E. Grand challenge commentary: Exploiting single-cell variation for new antibiotics. Nat. Chem. Biol. 6, 873–875 (2010).

    CAS  PubMed  Google Scholar 

  34. Winter, J.M., Behnken, S. & Hertweck, C. Genomics-inspired discovery of natural products. Curr. Opin. Chem. Biol. 15, 22–31 (2011).

    CAS  PubMed  Google Scholar 

  35. Gil-Turnes, M.S., Hay, M.E. & Fenical, W. Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246, 116–118 (1989). This provides an excellent example of the roles of metabolic exchange factors produced by symbiotic bacteria in host survival.

    CAS  PubMed  Google Scholar 

  36. Piel, J. Metabolites from symbiotic bacteria. Nat. Prod. Rep. 26, 338–362 (2009).

    CAS  PubMed  Google Scholar 

  37. Hentschel, U. et al. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68, 4431–4440 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Currie, C.R., Scott, J.A., Summerbell, R.C. & Malloch, D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398, 701–704 (1999).

    CAS  Google Scholar 

  39. Currie, C.R. et al. Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299, 386–388 (2003).

    CAS  PubMed  Google Scholar 

  40. Oh, D.C., Poulsen, M., Currie, C.R. & Clardy, J. Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat. Chem. Biol. 5, 391–393 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Schultz, T.R. & Brady, S.G. Major evolutionary transitions in ant agriculture. Proc. Natl. Acad. Sci. USA 105, 5435–5440 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Haeder, S., Wirth, R., Herz, H. & Spiteller, D. Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc. Natl. Acad. Sci. USA 106, 4742–4746 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Schoenian, I. et al. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc. Natl. Acad. Sci. USA 108, 1955–1960 (2011). This work used new methodologies to characterize the metabolic exchange between microbial communities within the nests of leaf-cutting ants.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Guarner, F. & Malagelada, J.R. Gut flora in health and disease. Lancet 361, 512–519 (2003).

    PubMed  Google Scholar 

  45. Grice, E.A. & Segre, J.A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Kau, A.L., Ahern, P.P., Griffin, N.W., Goodman, A.L. & Gordon, J.I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Valm, A.M. et al. Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc. Natl. Acad. Sci. USA 108, 4152–4157 (2011). This paper represents an example of the use of labeling and imaging approaches to visualize and differentiate phylotypes of microbial communities.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Rickard, A.H. et al. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60, 1446–1456 (2006).

    CAS  PubMed  Google Scholar 

  49. Schloss, P.D. & Handelsman, J. The last word: books as a statistical metaphor for microbial communities. Annu. Rev. Microbiol. 61, 23–34 (2007).

    CAS  PubMed  Google Scholar 

  50. Tringe, S.G. & Rubin, E.M. Metagenomics: DNA sequencing of environmental samples. Nat. Rev. Genet. 6, 805–814 (2005).

    CAS  PubMed  Google Scholar 

  51. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Baltz, R.H. Renaissance in antibacterial discovery from actinomycetes. Curr. Opin. Pharmacol. 8, 557–563 (2008).

    CAS  PubMed  Google Scholar 

  53. Moter, A. & Gobel, U.B. Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms. J. Microbiol. Methods 41, 85–112 (2000).

    CAS  PubMed  Google Scholar 

  54. de Jong, A., van Heel, A.J., Kok, J. & Kuipers, O.P. BAGEL2: mining for bacteriocins in genomic data. Nucleic Acids Res. 38, W647–W651 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Rausch, C., Weber, T., Kohlbacher, O., Wohlleben, W. & Huson, D.H. Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res. 33, 5799–5808 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Ansari, M.Z., Yadav, G., Gokhale, R.S. & Mohanty, D. NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res. 32, W405–W413 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Medema, M.H. et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal sequences. Nucleic Acids Res. 39, W339–W346 (2011). This paper describes the development of the most comprehensive software pipeline available at present that is capable of identifying potential biosynthetic gene clusters for the whole range of known secondary metabolite classes.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Watrous, J.D. & Dorrestein, P.C. Imaging mass spectrometry in microbiology. Nat. Rev. Microbiol. 9, 683–694 (2011). This thorough review covers IMS techniques and their applicability in microbiology.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Liu, W.T. et al. Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc. Natl. Acad. Sci. USA 107, 16286–16290 (2010). This is the first work to apply IMS to discover specific factors that are active in microbial intraspecies interactions.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Yang, Y.L., Xu, Y., Straight, P. & Dorrestein, P.C. Translating metabolic exchange with imaging mass spectrometry. Nat. Chem. Biol. 5, 885–887 (2009). This is the original report on the development of IMS to study microbial metabolic exchange.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Gonzalez, D. et al. Microbial competition between Bacillus subtilis and Staphylococcus aureus monitored by imaging mass spectrometry. Microbiology published online, doi:10.1099/mic.0.048736-0 (30 June 2011).

  62. Yang, Y.L. et al. Connecting chemotypes and phenotypes of cultured marine microbial assemblages by imaging mass spectrometry. Angew. Chem. Int. Edn. Engl. 50, 5839–5842 (2011). This paper highlights the utility of applying IMS to the investigation of metabolic exchange in microbial assemblages.

    CAS  Google Scholar 

  63. McLean, J.S. et al. Investigations of structure and metabolism within Shewanella oneidensis MR-1 biofilms. J. Microbiol. Methods 74, 47–56 (2008).

    CAS  PubMed  Google Scholar 

  64. McLean, J.S., Ona, O.N. & Majors, P.D. Correlated biofilm imaging, transport and metabolism measurements via combined nuclear magnetic resonance and confocal microscopy. ISME J. 2, 121–131 (2008).

    CAS  PubMed  Google Scholar 

  65. Boedicker, J.Q., Vincent, M.E. & Ismagilov, R.F. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Edn. Engl. 48, 5908–5911 (2009).

    CAS  Google Scholar 

  66. Kersten, R.D. et al. A mass spectrometry-guided genome mining approach for natural product peptidogenomics. Nat. Chem. Biol. 7, 794–802 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. De Sordi, L. & Muhlschlegel, F.A. Quorum sensing and fungal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Res. 9, 990–999 (2009).

    CAS  PubMed  Google Scholar 

  68. Shank, E.A. & Kolter, R. New developments in microbial interspecies signaling. Curr. Opin. Microbiol. 12, 205–214 (2009). This review focuses on how bacterial small molecules modulate interspecies interactions.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Craig, L., Pique, M.E. & Tainer, J.A. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2, 363–378 (2004).

    CAS  PubMed  Google Scholar 

  70. Proft, T. & Baker, E.N. Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease. Cell. Mol. Life Sci. 66, 613–635 (2009).

    CAS  PubMed  Google Scholar 

  71. Dubey, G.P. & Ben-Yehuda, S. Intercellular nanotubes mediate bacterial communication. Cell 144, 590–600 (2011).

    CAS  PubMed  Google Scholar 

  72. Gorby, Y.A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl. Acad. Sci. USA 103, 11358–11363 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).

    CAS  PubMed  Google Scholar 

  74. DiGiuseppe Champion, P.A. & Cox, J.S. Protein secretion systems in Mycobacteria. Cell. Microbiol. 9, 1376–1384 (2007).

    Google Scholar 

  75. Hayes, C.S., Aoki, S.K. & Low, D.A. Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 44, 71–90 (2010). This comprehensive review discusses the contact-dependent systems that microbes use to interact with each other and their environment.

    CAS  PubMed  Google Scholar 

  76. Holland, I.B. The extraordinary diversity of bacterial protein secretion mechanisms. Methods Mol. Biol. 619, 1–20 (2010).

    CAS  PubMed  Google Scholar 

  77. Natale, P., Bruser, T. & Driessen, A.J. Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane–distinct translocases and mechanisms. Biochim. Biophys. Acta 1778, 1735–1756 (2008).

    CAS  PubMed  Google Scholar 

  78. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S.C. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171–184 (2010).

    CAS  PubMed  Google Scholar 

  79. Ubbink, J. & Schar-Zammaretti, P. Probing bacterial interactions: integrated approaches combining atomic force microscopy, electron microscopy and biophysical techniques. Micron 36, 293–320 (2005).

    CAS  PubMed  Google Scholar 

  80. Haurat, M.F. et al. Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 286, 1269–1276 (2011).

    CAS  PubMed  Google Scholar 

  81. Mashburn, L.M. & Whiteley, M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422–425 (2005).

    CAS  PubMed  Google Scholar 

  82. Roze, L.V., Chanda, A. & Linz, J.E. Compartmentalization and molecular traffic in secondary metabolism: a new understanding of established cellular processes. Fungal Genet. Biol. 48, 35–48 (2011).

    CAS  PubMed  Google Scholar 

  83. Kai, M. et al. Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81, 1001–1012 (2009).

    CAS  PubMed  Google Scholar 

  84. Minerdi, D., Bossi, S., Gullino, M.L. & Garibaldi, A. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ. Microbiol. 11, 844–854 (2009).

    CAS  PubMed  Google Scholar 

  85. Schulz, S. & Dickschat, J.S. Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24, 814–842 (2007).

    CAS  PubMed  Google Scholar 

  86. Borges-Walmsley, M.I. & Walmsley, A.R. cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. Trends Microbiol. 8, 133–141 (2000).

    CAS  PubMed  Google Scholar 

  87. Boyer, M. & Wisniewski-Dye, F. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70, 1–19 (2009).

    CAS  PubMed  Google Scholar 

  88. Pesavento, C. & Hengge, R. Bacterial nucleotide-based second messengers. Curr. Opin. Microbiol. 12, 170–176 (2009).

    CAS  PubMed  Google Scholar 

  89. Ratcliff, W.C. & Denison, R.F. Microbiology. Alternative actions for antibiotics. Science 332, 547–548 (2011). This article discusses the possibility that there may be several roles for antibiotics in the native environment of microbes.

    CAS  PubMed  Google Scholar 

  90. Singh, A. & Del Poeta, M. Lipid signalling in pathogenic fungi. Cell. Microbiol. 13, 177–185 (2011).

    CAS  PubMed  Google Scholar 

  91. Vendeville, A., Winzer, K., Heurlier, K., Tang, C.M. & Hardie, K.R. Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3, 383–396 (2005).

    CAS  PubMed  Google Scholar 

  92. Putman, M., van Veen, H.W. & Konings, W.N. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 64, 672–693 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Boyd, E.F. & Brussow, H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10, 521–529 (2002).

    CAS  PubMed  Google Scholar 

  94. Coleman, D.C. et al. Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of beta-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J. Gen. Microbiol. 135, 1679–1697 (1989).

    CAS  PubMed  Google Scholar 

  95. Kuroda, M. et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225–1240 (2001).

    CAS  PubMed  Google Scholar 

  96. Flemming, H.C. & Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010).

    CAS  PubMed  Google Scholar 

  97. Kearns, D.B. & Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49, 581–590 (2003).

    CAS  PubMed  Google Scholar 

  98. López, D., Vlamakis, H., Losick, R. & Kolter, R. Cannibalism enhances biofilm development in Bacillus subtilis. Mol. Microbiol. 74, 609–618 (2009).

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to acknowledge J. Yang, W. Moree and C. Rath (University of California, San Diego) for providing critical reviews of the manuscript and E. Shank (Harvard Medical School) for insightful discussions. The P.C.D. laboratory is supported by US National Institutes of Health grants GM094802, GM086283 and AI095125 and by the Beckman Foundation. The K.P. laboratory is supported by US National Institutes of Health grants GM057045 and AI095125.

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Phelan, V., Liu, WT., Pogliano, K. et al. Microbial metabolic exchange—the chemotype-to-phenotype link. Nat Chem Biol 8, 26–35 (2012). https://doi.org/10.1038/nchembio.739

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